He directed and co-wrote with his brother Tom the film Birthday Girl (2001), which was produced by his brother Steve and starred Nicole Kidman.[4]

Butterworth received positive reviews of his play The Night Heron, which premiered in the West End at the Royal Court Theatre in 2002. The Guardian reviewer wrote: "Can a play be simultaneously very good and very bad? I believe so."[5]The Winterling also ran at the Royal Court in 2006. The britishtheatreguide wrote: "The Winterling can be a difficult play but contains rich veins of comedy."[6]

Butterworth's fourth play for the Royal Court Theatre was Jerusalem, which premiered in July 2009 to positive reviews. Described as a "contemporary vision of life in [England's] green and pleasant land", Jerusalem was the second important Butterworth production in London in 2009.[8] The production starred Mark Rylance as Johnny Byron, and featured Mackenzie Crook as Ginger in a supporting role. It was a sell-out at the Royal Court, won the Evening Standard Theatre Award and Critics' Circle Theatre Award for the best play of 2009 and, with the same cast, transferred to the Apollo Theatre on Shaftesbury Avenue in January 2010. Jerusalem opened on Broadway in April 2011, with many of the original UK cast.[9] It returned to London later that year, again playing at the Apollo. In January 2014 Jerusalem opened at the San Francisco Playhouse, where it also received rave reviews.[10]Jerusalem was nominated for the 2011 Tony Award, Play[11] and Mark Rylance won the 2011 Tony Award for Best Performance by an Actor in a Play.[9]

Butterworth's play The Ferryman opened at the Royal Court Theatre in April 2017. Directed by Sam Mendes,[16] it became the fastest selling play in the Royal Court Theatre's history.[17] Set in Rural Derry in 1981 and focussing on the events surrounding the deaths of the IRA hunger strikers, it received 15 five-star reviews, including all the major UK papers. The Irish Times said "Although Butterworth is English, The Ferryman feels like a thoroughly Irish play, not only because there is not a single false note in the dialogue." The Huffington Post called it "one of the two or three greatest plays of the decade". However, The Guardian 's Sean O'Hagan wrote "I'm from Northern Ireland and it doesn't ring true" and it was "so close to a cultural stereotype as to be offensive".[18] Two weeks later The Irish Times printed an article by Father Ted actor Gerard Lee[19] entitled "In defence of The Ferryman" which challenged negative comments, calling the play "layered and powerful".[20]